SMOKING AND PERIODONTAL DISEASE

D.F. Kinane*
I.G. Chestnutt
Periodontology and Oral Immunology, University of Glasgow Dental Hospital and School, 378 Sauchiehall Street, Glasgow, G2 3JZ, Scotland, UK; *corresponding author
ABSTRACT: Numerous investigations of the relationship between smoking and periodontal disease have been per-
formed over the last 15 years, and there now exists a substantial body of literature upon which this current review is
based. From both cross-sectional and longitudinal studies, there appears to be strong epidemiological evidence that
smoking confers a considerably increased risk of periodontal disease. This evidence is further supported by the data
emanating from patients who stop smoking. These patients have levels of risk similar to those of non-smokers.
Numerous studies of the potential mechanisms whereby smoking tobacco may predispose to periodontal disease have
been conducted, and it appears that smoking may affect the vasculature, the humoral immune system, and the cellular
immune and inflammatory systems, and have effects throughout the cytokine and adhesion molecule network. The aim
of this review is to consider the evidence for the association between smoking and periodontal diseases and to high-
light the biological mechanisms whereby smoking may affect the periodontium.
Key words. Smoking, cessation, nicotine, immunoglobulins, cytokines, periodontitis

(I) Introduction not smoke, with odds ratios ranging from 3.25 to 7.28 for
The concept that smoking tobacco may be prejudicial to light and heavy smokers, respectively (Grossi et al., 1995).
periodontal health is not new, an association between In a Swedish investigation of 155 patients with perio-
acute necrotizing ulcerative gingivitis and smoking having dontal disease, a significantly higher percentage were
been observed in the late 1940s (Pindborg, 1947). In the found to be smokers than in the population at large, and
interim, numerous investigations of the relationship the risk ratio was reported as 2.5 (Bergstrom, 1989).
between smoking and the various other forms of perio- After controlling for confounding factors such as
dontal disease have continued, and there now exists a age, sex, plaque, and calculus, in a study of 615 American
substantial body of literature upon which this current adults, the odds of having a mean probing depth of at
review is based. least 3.5 mm in one randomly selected posterior sextant
The purpose of this review is: (1) to examine evi- was reported as five times greater for smokers than for
dence for the association between smoking and perio- non-smokers (Stoltenberg et al., 1993).
dontal disease; (2) to discuss possible biological mecha- In 1991, a radiographic study of alveolar bone loss in
nisms whereby smoking may adversely affect the perio- Swedish dental hygienists demonstrated that the distance
dontium; and (3) to consider the impact of smoking on between the cemento-enamel junction and the interdental
periodontal treatment. septum was significantly greater in smokers than in non-
smokers and increased with increasing smoking exposure.
(11) Epidemiology This study, in adults with good oral hygiene, suggested
that smoking-related bone loss was not simply correlated
(A) STRENGTH OF ASSOCIATION with plaque levels (Bergstrom et al., 1991). A more recent
The stronger an association between a given factor and a study of 540 Swedish adults 20-70 years of age has
disease, the more likely this factor will implicated as a revealed that the three variables smoking, greater age, and
risk factor. The strength of an association in both case- higher mean plaque levels were potential risk factors for
control and prospective studies can be measured by the severe periodontitis (Norderyd and Hugoson, 1998).
relative risk, which is often expressed in terms of the A case-control study of the relationship between
odds ratio. Numerous cross-sectional studies on the life-events and periodontitis has shown smoking to be
effect of smoking on periodontal health have been statistically associated with periodontal disease, after
reported, with odds ratios generally in the order of 2 to 6. controlling for oral health behavior and socio-demo-
One of the largest studies of risk factors for perio- graphic variables (Croucher et al., 1997). This work con-
dontal disease was that undertaken in Erie County, New firmed the earlier findings that periodontal disease expe-
York State. Involving 1361 subjects aged 25 to 74 years, rience is influenced by social and behavioral factors, and
this study showed that those who smoked were at greater that smoking status was independent of other factors
risk for experiencing severe bone loss than those who did studied (Locker and Leake, 1993).

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356 Crit Rev

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 In an investigation of behavioral and socio-demo-
graphic risk indicators of attachment loss in 873 subjects,
aged at least 45 years, smoking was significantly associ-
ated with a higher probability of having one or more
periodontal sites with severe attachment loss (Dolan et
al. 1997). Smoking was found to be the strongest inde-
pendent factor affecting periodontal status in 499 Finnish
male industrial workers (Ahlberg et al., 1996).
Although most studies report smoking to increase
the risk of periodontal disease in the order of two- to six-
fold, a study carried out in Northern Ireland suggested
that the odds ratio for established periodontitis in a
group of 82 young subjects (20 to 30 years of age) who
regularly attended their dentist was as high as 14.1
(Linden and Mullally, 1994). Further evidence of the par-
ticularlv damaging effects of smoking on periodontal
health in younger people was reported in a Swedish
study. This longitudinal study investigated tooth loss in
273 individuals who were followed for a ten-year period.
The risk attributable to smoking in younger males smo-
king more than 15 cigarettes per day was reported as 78%
(Holm, 1 994 This is given further weight by the findings
of Haber and colleagues, who, in determining the role of
smokincg as a risk factor for periodcntitis in diabetic and
non-diabetic study groups, suggested that in the non-
diabetic group 51.% of the periodontitis in the 19-30-
year-olds and 32°o in those aged 31 to 40 years were
associal-ed with smoking (Haber et c1l., 1993).
Although the greatest number of investigations of
the relationship between smoking and periodontal dis-
ease are c ross-sectional, a few longitudinal investiga-
tions have also been conducted. In a ten-year longitudi-
nal radiographic study of alveolar bone loss which began
in 1970, it was shown that in those subjects who had at
least 2(0 teethi it the start of the study, smoking was a sig-
nificant predictor of future bone loss (Bolin, 1986), and
in a five-year study of attachment loss in 800 communi-
ty-dwelling adults, smokers were found to be at an
increased risk for attachment loss (Beck et al., 1997).
A further longitudinal study, in which a wide range
of clinical microbiological, and immunological indica-
tors was correlated with disease progression, reported
that over the one-year period of the investigation, smo-
kers exhibited both greater attachment loss and bone
loss when compared with their non-smoking counter-
parts. Smokers were shown to be at significantly greater
risk for further attachment loss when compared with
non-smokers, the odds ratio being quoted as 5.4
iMachtei et aii. 1997).
(B) CONSISTENCY OF OBSERVATIONS
While many of the initial studies on the relationship
between smoking and periodontal disease reached con-
flicting and contradictory conclusions, in retrospect, such
findings can be explained by the failure to account suffi-
ciently for the multifactorial nature of periodontal dis-
ease. The ambiguity that clouded the early studies on the
role of smoking ir periodontal disease has been resolved
((33636
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1(3).356-365 i20001
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by an array of studies with well-defined clinical criteria
and more sophisticated data analysis (Mandel, 1994)1
(C) DOSE-RESPONSE
In determining attributable risk, it is of value to examine
the relationship between the degree of exposure to an
alleged risk factor and disease prevalence. The ability to
demonstrate a dose-response strengthens the evidence
of risk factor status. However, the absence of a dose-
response relationship does not necessarily rule out a
causal relationship, since a threshold may exist above
which disease develops.
Grossi et al. (I1994) examined the relationship between
smoking and attachment loss and demonstrated a dose-
dependent response, the odds for more severe attachment
loss in smokers, compared with non-smokers, ranging
from 2.05 for light smokers to 4.75 in heavy smokers. These
findings support those of Alpagot and colleagues, who
reported that probing depth was significantly correlated
with 'packyears' (i.e., packs of cigarettes smoked per day
multiplied by the number of years the subject has smoked)
(Alpagot et cl., 1996). Furthermore years of exposure to
tobacco products have been shown to be a statistically sig-
nificant risk factor for periodontal disease in 1 156 commu-
nity-dwelling New England elders, regardless of other
social and behavioral factors ((ette et al. 19931.
A Spanish survey involving 889 patients reported
that gingival recession, pocket depth, and probing
attachment level were significantly related to smoking
status, and that attachment levels were proportionate to
the quantity of cigarettes smoked. Smoking one cigarette
per day, up to ten, and up to 20, increased probing attach-
ment level by 0.5%, 500, and 10o, respectively. However,
only in the latter group did loss of attachment differ sig-
nificantly from that of non-smokers This led the authors
to conclude that tobacco usage increases disease sever-
ity, and that this effect is clinically evident above a cer-
tain level of usage (Martinez-Canut et crl, 1 995).
This suggestion of greater periodontal destruction
above a certain level of smoking was suggested in a pre-
vious investigation of alveolar bone loss. Expressed as a
percentage of tooth root length in 723 dentate adults,
alveolar bone height was shown to be significantly lower
in individuals smoking more than 5 g of tobacco per day
compared with those smoking between I and 5 g of
tobacco per day (Wouters et cl., 1993). Norderyd and
Hugoson (1998) examined 547 Swedish adults and
found that moderate to heavy smoking (greater thar or
equal to 10 cigarettes per day) was associated with
severe periodontitis, but that light smoking (fewer than
10 cigarettes per day) was not.
The strong association found between smoking
and advanced periodontitis is consistent with the
hypothesis that smoking has cumulative detrimental
effects on periodontal health (Horning et r1- 1992).
Thus, there is good evidence that the more a patient
smokes, the greater the degree of periodontal disease
that will be experienced. Furthermore, there is a sug-
Gi e Oa il e
357
Crit Rev Oral Biot Med
gestion that this may worsen above a certain threshold.
It is difficult to determine the strength of smoking
as a risk factor, since a problem lies in accurate mea-
surement of a subject's exposure to tobacco products
over many years, and to date, most studies on the rela-
tionship between smoking and periodontal disease have
determined smoking status by interview or question-
naire. However, it should be remembered that all retro-
spective studies are subject to recall bias, and while
some studies have quantified lifetime exposure in pack-
years, current levels of smoking may not reflect past
exposure. In one of the few studies which, to date, have
measured cotinine, the severity of periodontal destruc-
tion, measured either as clinical attachment level or
crestal bone height, was shown to be statistically posi-
tively correlated with serum cotinine levels (Gonzalez et
al., 1996). Cotinine is the principle metabolite of nicotine
and as such provides a valuable quantitative measure of
smoking status. Patients' cotinine levels have recently
been shown to correlate directly with outcomes of pro-
gressive periodontal breakdown (Machtei et al., 1997).
(D) SUBGINGIVAL MICROBIAL FLORA
Analysis of the available data suggests that smokers may
have a more 'pathogenic' microbial flora, in that
Bacteroides forsythus was harbored subgingivally more in
smokers than in non-smokers (Zambon et al., 1996).
There was also a tendency for Porphyromonas gingivalis
counts to be higher in smokers than in non-smokers, but
this failed to reach significance. The data were adjusted
for attachment loss and age, and thus the reported B.
forsythus increase in smokers (former and current) is not
simply because they have more severe periodontal dis-
ease. Similarly, current smokers have elevated
Actinobacillus actinomycetemcomitans and B. forsythus counts,
even after adjustments for periodontal disease and age.
The finding of elevated levels of particular pathogens
tends to vary across different studies. A more recent
study using molecular analyses techniques for six puta-
tive periodontal pathogens found that current smokers
displayed an increased risk for harboring Treponema denti-
cola (OR = 4.61) (Umeda et al., 1998).
Haffajee et al. (1997) have reported significant clini-
cal improvements, following scaling and root planing
(SRP), in subjects who had never smoked or who were
past smokers, but not in current smokers. P. gingivalis, B.
forsythus, and Treponema denticola were equally prevalent
among current, past, and "never" smokers before therapy
and decreased significantly post-SRP in all but the cur-
rent smokers. Clinical improvement post-SRP in all
patients was accompanied by a modest change in the
subgingival microbiota, primarily reductions in P. gingi-
valis, B. forsythus, and T. denticola.
Stoltenberg et al. (1993) studied periodontitis
patients to determine if the prevalence of 5 bacteria com-
monly associated with periodontal disease differed
between smokers and non-smokers. They studied P. gin-
givalis, A. actinomycetemcomitans, Prevotella intermedia, Eikenella
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corrodens, and Fusobacterium nucleatum. No statistically sig-
nificant difference in the prevalence of any of the bacte-
ria was found between smokers and non-smokers. The
investigators performed a logistic regression analysis on
the data and found that smoking and mean probing
depth > 3.5 mm were significantly associated with the
presence of A. actinomycetemcomitans, P. intermedia, and E.
corrodens (P < 0.05).
(E) CESSATION
Further evidence of the role of smoking in periodontal
disease comes from studies of patients who stop smo-
king. If smoking is associated with increased risk for perio-
dontal disease, a reduction or elimination of tobacco use
should reduce this risk and should be beneficial to the
patient. There is good evidence that the prevalence of
periodontal disease is less in former smokers than in
those who continue to smoke.
In a study comparing the prevalence of cigarette
smoking among patients attending specialist perio-
dontal and general dental practices, a dose-response
was observed. After controlling for age and sex, the odds
ratio for those who currently smoked compared with
"never" smokers was 3.3, while former smokers compared
with "never" smokers had a ratio of 2.1 with regard to the
presence of moderate or advanced periodontitis (Haber
and Kent, 1992). The prevalence and severity of perio-
dontitis have been shown to be less in former smokers
compared with current smokers, leading Haber to con-
clude that stopping smoking is beneficial (Haber, 1994).
In a ten-year radiographic follow-up of alveolar
bone loss, it was reported that progression of bone loss
was significantly retarded in those who had given up
smoking during the study, compared with those who con-
tinued to smoke (Bolin et al., 1993).
Prospective observations of tooth loss in 248
women and 977 men, with a mean follow-up time of six
years, indicated that individuals who continued to
smoke cigarettes had in the order of 2.4- to 3.5-fold risk
of tooth loss compared with non-smokers. The rates of
tooth loss in men were significantly reduced after they
quit smoking cigarettes, but remained higher than those
in non-smokers. The authors concluded that stopping
smoking significantly benefits an individual's likelihood
of tooth retention, but it may take decades for the indi-
vidual to return to the rate of tooth loss observed in
non-smokers (Krall et al. 1997).
Summary
Cross-sectional and longitudinal studies have indicated a
strong relationship between smoking and increased risk
for periodontal breakdown. Research performed in the
last decade has proved beyond doubt that smokers have
more periodontal problems than non-smokers. The evi-
dence that smoking is a risk factor for periodontal disease
is strengthened by the consistency of findings in different
studies and in different populations, viz. North America,
the Nordic countries, and the United Kingdom. There are
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Biol Med 11(3):356-365 (2000)
inconsistencies, however, in the studies reporting the
most frequently detected pathogers in periodontal pock-
ets of smokers. Pocket microflora differences between
smokers and non-smokers appear to be largely study-
dependent, and little can be inferred from these studies
on whether a specific microbial flora can increase the risk
or be associated with periodontal disease in smokers. The
strong epidemiological evidence that smoking confers an
increased risk of periodontal disease is further supported
bv evidence emanating from studies of patients who
stopped smoking. The prevalence of periodontal disease
is less in former smokers than in those who continue to
smoke indicating a clear advantage to those stopping
smoking in the benefit to periodontal health.
(111) Biological Effects of Smoking
in Periodontal Disease
Numerous studies of the potential mechanisms whereby
smoking tobacco may predispose to periodontal disease
have been conducted. A comprehensive review on the
modifying effects of tobacco and smoking on the host
immune and inflammatory response has been recently
published (Barbour et al., 1997). This section will focus on
the tissue effects of tobacco smoking peculiar to the
periodontal tissues, and on the clinical conditions, and
reviews the most periodontally relevant aspects of the
host-microbe interactions influenced by smoking. The
reader is referred to the in-depth host-response review
by Barbour et'al. ( 1997) for the more specific and general
systemic effects of smoking on the immune and inflam-
matorv systems.
(A) EFFECT OF NICOTINE
ON THE PERIODONTAL TISSUES
Nicotine may cause a vasoconstriction in the peripheral
blood vessels (Clarke et al., 1981) and thus may reduce the
clinical signls of gingivitis. Evidence for this reduction in
clinical disease expression comes from various sources,
including Bergstrom (19901, who compared the compli-
ance of smokers with that of non-smokers in an oral
hygiene intervention program. The plaque index
decreased in both groups, and, despite the similarity in
plaque index, gingival bleeding was significantly lower in
smokers than in non-smokers. These results suggest that,
in smokers, the clinical expression of gingivitis (i.e., chron-
ic inflammation) in response to plaque is suppressed.
A stucdy with similar findings was conducted by
Danielsen et al (1990), who set up an experimental gin-
givitis studv on smokers and non-smokers. Similar
amounts of plaque accumulated in the two groups dur-
ing the period of no oral hygiene, but clinically, smokers
exhibited less gingival inflammation than non-smokers.
A study by Holmes (1990) compared crevicular fluid flow
in smokers and non-smokers with clinically healthy gin-
giva and the crevicular fluid flow of smokers in the areas
physically exposed to smoke (maxillary lingual) and in
areas not physically exposed to smoke (maxillary buc-
cal). Smokers had significantly less crevicular fluid flow
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than non-smokers. Interestingly, the exposed lingual
areas of smokers showed no significant difference from
the less exposed buccal areas, which suggests that the
effect of nicotine may not be local or, if it is local, that it
may be modified by the saliva and its effects dispersed.
The authors suggest that the effect of tobacco smoke on
clinically healthy gingiva may be through vasoconstric-
tion rather than direct physical irritation.
Kinane and Radvar 11997), investigating the
responses of smokers and non-smokers, with and with-
out subgingival antimicrobials, to instrumentation, also
reported that gingival crevicular fluid (GCF) volumes
were significantly lower among smokers than non-smo-
kers. In this study, it was noted that, after therapy, the
decrease in the GCF volume of smokers was less than
that of non-smokers, regardless of treatment modality.
However, the actual mean GCF volumes still remained
lower in smokers than in non-smokers. These findings
are consistent with a diminished peripheral blood flow
leading to a diminished GCF flow.
(B) EFFECT OF NICOTINE ON THE IMMUNE
AND INFLAMMATORY SYSTEMS
Smoking has been shown to affect various aspects of the
host immune response (AAP, 1996). Smoking may have
an adverse effect on fibroblast function (Raulin et al.,
1988), chemotaxis and phagocytosis by neutrophils
(Kenney et al., 1977; Kraal et al., 1977), and immunoglob-
ulin production (Holt, 1987; Johnson et al., 1990). To
mount a successful response to the bacteria, immune
cells must arrive at the inflammatory site in appropriate
numbers. Nicotine increases intercellular adhesion mol-
ecule-I (ICAM-I) and endothelial leukocyte adhesion
molecule-l (ELAM- ) on human umbilical vein cells
(endothelial cells) and appears to increase soluble
ICAM- I in the serum of smokers (Koundouros et al.,
19961. These adhesion molecule changes may affect
leukocyte binding to endothelial cells lining the capillar-
ies and post-capillary venules and thus, may impede the
recruitment of important host defense cells to the area of
inflammation and microbial challenge.
Alavi et al. (1995) compared elastase concentrations
in the GCF from individual sites of smokers with those in
the GCF of non-smokers. They found that smokers had
lower elastase concentrations in GCF than did non-
smokers. The reasons for this are not immediately clear.
Elastase is produced locally mainly by the polymor-
phonuclear leukocyte (PMN) cells and is not found in
normal serum. Thus, vasoconstriction of blood vessels
would not account for the decrease in GCF elastase con-
centration in non-smokers. It may be that PMNs are less
functional (Wolff et al., 1994) or are present in reduced
quantities in the gingival crevices of smokers due to the
reduced vascularity of the region.
(C) CYTOKINES AND SMOKING
Recent reports suggest that host cytokine levels are influ-
enced by smoking. Tappia et a1.) 11995) have shown that the
5
Crit Rev Oral Biol Med 359
plasma responses of smokers following lipopolysaccha-
ride stimulation differed from those of non-smokers, in
that smokers had significantly more tumor necrosis factor
alpha (TNFa-) and Interleukin-6 (IL-6) and also the acute-
phase protein ox2-macroglobulin. Bostrom et al. (1998b)
have reported that smokers had significantly higher TNFx
levels in their GCF than did non-smokers in untreated and
treated periodontitis patients (Bostrom et al., 1998a,b).
Kuschner et al. (1996) have reported a dose-dependent
effect of smoking on IL- 1, IL-6, IL-8, and monocyte
chemotactic protein (MCP)- I levels.
In contrast to these studies, Madretsma et al. (I1996)
have suggested that nicotine exerts a negative
immunoregulatory effect through modulation of the
cytokine production of mononuclear cells. The inhibitory
effects of nicotine on IL-2 and TNFot production are simi-
lar to those seen for prednisolone (an established anti-
inflammatory steroid). In this study, the nicotine concen-
trations giving these anti-inflammatory effects fell within
the normal plasma nicotine range of smokers. A further
study by Bernzweig et al. (1998) found that levels of IL-113
from gingival mononuclear cells were decreased when
these cells were exposed to nicotine. This last study, how-
ever, used unrealistically high levels of nicotine, approxi-
mately 75 times that of the mean saliva level of nicotine
found in smokers. These in vitro studies on nicotine's
effects on cell cytokines and the cytokine levels in patient
smokers appear to be in conflict. These differences need
to be investigated by careful clinical and laboratory stud-
ies which also consider that smoking's effects are more
complex than just increasing the nicotine concentration,
and that the concentrations of nicotine and the other
chemicals and noxious stimuli related to smoking should
be factored into the studies. These studies may have
importance, given the weight currently being given to the
theories that cytokine overproduction may be a detri-
mental host response which predisposes an individual to
periodontitis (Kornman and di Giovine, 1998).
(D) SMOKING AND THE HUMORAL IMMUNE RESPONSE
Several recent papers and reviews have suggested that
existing risk and prevention models would be strength-
ened by the inclusion of data on host-defense mecha-
nisms (Genco, 1992; Page, 1992; Haber, 1994; Quinn et al.,
1996). Macrophages play important roles in both cell-
mediated and humoral immunity as antigen-presenting
cells. However, antigens are presented in the context of
class 11 major histocompatibility complex (MHCII) surface
molecules. It has been shown that alveolar macrophages
from smokers exhibit reduced expression of class II MHC
(Pankow et al., 1991; Mancini et al., 1993). This may even-
tually lead to a reduction in the humoral immune
response to invading organisms. Smoking has been
shown to reduce the concentration of serum IgG general-
ly (Ferson et al., 1979; Gulsvik and Fagerhol, 1979;
Anderson et al., 1982; Hersey et al., 1983; Robertson et al.,
1984; McSharry et al., 1985). Interestingly, seroconversion
following hepatitis B vaccine occurs much more slowly in
360
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smokers than in non-smokers, and the frequency of sub-
jects undergoing an immune response is lower for smok-
ers (Struve et al., 1992; Roome et al., 1993).
More specifically, smokers have been shown to have
reduced titers of serum IgG to P. intermedia and F. nuclea-
tum (Haber, 1994). Quinn et al. (1996) have recently
demonstrated that smoking tends to limit the produc-
tion of IgG2 in generalized early-onset periodontitis
(GEOP) patients. This is significant in that this isotype is
associated with the humoral immune response against
carbohydrate antigens commonly found on oral
pathogens (Ling et al., 1993). Moreover, it has recently
been shown that the level of IgG2 against A. actino-
mycetemcomitans is lower in smokers than in non-smokers
among EOP patients (Tangada et al., 1997).
Gunsolley et al. (1997) have shown that smoking
modifies the concentrations of some lgG subclasses in
specific racial and diagnostic groups. In Blacks who
smoked, those with chronic adult periodontitis had lower
IgG1, while those with generalized early-onset periodon-
titis had lower IgG2. In White subjects, complex relation-
ships between smoking and allotypic markers were
noted, but no influence of periodontal diagnosis was
found. Thus, in addition to immunoglobulin allotype,
smoking in Blacks appears to influence their IgG sub-
class concentrations. Thus, smoking may alter the type of
humoral immune response seen.
Summary
It is suggested by several studies that smokers may have
more disease because their microbial flora may be more
'pathogenic'. However, host-related factors must influ-
ence this subgingival niche and the microflora therein.
The host defense system will include the soluble and cel-
lular components of the inflammatory and immune sys-
tems as well as the innate immunity afforded by such
things as the epithelial barrier and fluid flow (GCF and
saliva). The reduced GCF flow reported in smokers will
mean that antibodies and other defense molecules
derived from the serum will be reduced in quantity. A fur-
ther consequence of reduced GCF flow would be fewer
microbial nutrients and less flushing of the gingival
crevice and removal of microbes and waste products as
the GCF leaves the gingival crevice by the positive out-
ward flow. These factors may all influence the flora at
these sites. Smoking may affect the vasculature, the
humoral immune system, and the cellular and soluble
inflammatory system, and may have effects throughout
the cytokine and adhesion molecule network. The rela-
tive importance of these smoking-related alterations and
their precise mode of action in increasing the risk of
periodontal disease remains to be elucidated.
(IV) Smoking and Periodontal Treatment
(A) RESPONSE TO CONVENTIONAL TREATMENT
The present literature suggests that the outcome in
smokers is less favorable than in non-smokers. Ah et al.
Grit Rev
Crit Rev Oral
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11(3):356-365 (2000)
 (1994j have demonstrated a poorer response to perio-
dontal treatment in smokers compared with non-smo-
kers. Preber and Bergstrbm (I 990) found that, 12 months
following surgery, smokers had a statistically significant-
ly reduced probing depth reduction compared with non-
smokers, despite accounting for differences in levels of
plaque accumulation.
Preber et uil. ( 1995) studied the clinical and microbio-
logical effects of non-surgical therapy and found that
smokers had a less favorable outcome in terms of pocket
depth reduction than did smokers. The study revealed no
difference, however, between smokers and non-smokers
in terms of the microbiological changes following thera-
py, i.e., the microflora was broadly similar in both cate-
gories of patients before and after treatment. Machtei et
al. 1998) considered the changes in attachment level and
alveolar bone levels approximately one year after the
hygiene phase of therapy. Non-smokers had relatively sta-
ble bone height, whereas smokers exhibited an annual-
ized rate of bone loss of 1. 17 mm. Furthermore, in a
recent five-year study (Bostrom et al., 1998a), were found
to exhibit less improvement compared with non-smokers
in terms of bone height.
Approximately 90% of patients who were catego-
rized as having failed to respond to conventional therapy
were smokers (MacFarlane et al., 1992; Wolff et al., 1994).
Recent work by Colombo et l. (1998) has disagreed with
this stated proportion, since these investigators found
that only 25, of their patients were current smokers, but
that 40%, were former smokers. Bostrom et al. (1 998a) sug-
gested that former smokers often begin smoking again,
and therefore one must interpret the status of the former
smokers cautiously, since self-reporting of smoking sta-
tus is not reliable (Gonzalez et al., 996).
Although smokers will also benefit from treatment,
albeit to a lesser degree, treatment failures tend to pre-
dominate among smokers. Kinane and Radvar (1997)
found that the response to non-surgical mechanical
therapy is particularly poor in deep pockets in smokers.
Although the attachment gain was also greater among
the non-smokers than the smokers, this was not signifi-
cant. This indicates that, after treatment, a greater
degree of recession occurred among the non-smokers
compared with the smokers. In the description of the
appearance of smokers' periodontal condition, and in
studies looking cross-sectionally at smokers, a common-
lv noted feature is the level of recession, which is often
noted as worse in smokers than in non-smokers
(Martinez-Canutt et a., 1995; Gunsolley et al., 1998).
(B) RESPONSE TO MORE COMPLEX TREATMENT
Tonetti et cr1L. 11995) performed a retrospective study that
examined the effect of cigarette smoking on the healing
responise following guided tissue regeneration (GTR) in
deep .nfrabony defects. This study indicated that smo-
king was a significant factor in determining the clinical
outcome. A risk-assessment analysis indicated that smo-
kers had a -gnificantly greater likelihood than non-
11i3
56365200)
I 3 )3556- 365 -20)0
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smokers of having a reduced probing attachment level
gain following GTR. More recent studies have concurred
with these findings (Cortellini et al., 1996. Trombelli and
Scabia, 1997; Trombelli et al., 1997), and other investiga-
tors, when using regenerative procedures with allografts,
have also found smoking to be detrimental to healing
(Luepke et al., 1997; Rosen et al, 1996)
Haas et al. (I 996) looked at the relationship between
smoking and peri-implantitis. They found no significant
difference between smokers' and non-smokers' mean
maxillary and mandibular plaque indices. However, the
smokers had higher bleeding indices and mean peri-
implant pocket depths, and greater peri-implant muco-
sal inflammation mesial and distal to the implant. These
observations were significantly higher in the maxilla of
the smoking group than in the mandibles and in the
maxilla of the non-smokers (p < 0.01). These findings
suggest that implants placed in smokers have a greater
risk of developing peri-implantitis than those in non-
smokers, particularly in the maxilla.
(C) EFFECTS OF STOPPING SMOKING
ON PERIODONTAL TREATMENT
The effect of stopping smoking on response to treatment
is interesting. Kaldahl et al. (1996) have suggested that
past smokers and non-smokers responded similarly to
treatment. In addition, heavy smokers (over 20/day) had
higher plaque levels during maintenance and the poor-
est response to treatment, but did not significantly differ
from light smokers. A further study by Grossi et al. ( 1997)
investigated the effect of cigarette smoking on patients'
clinical and microbiological responses to mechanical
therapy. Current smokers had less healing and reduction
in subgingival B. forsythus and P. gingirzalis after treatment
compared with former and non-smokers. These authors
concluded that, since the healing and microbial respon-
ses of former smokers are comparable with those of non-
smokers, smoking cessation may restore the normal
periodontal healing response. Clearly, stopping smoking
is beneficial, but compliance with the smoking cessation
regime is often dubious with these patients. Future stud-
ies should monitor the amount smoked by assaying
serum cotinine, since patient compliance and self-
reporting are unreliable (Gonzalez et al. 19961.
(D) HEALING IN SMOKERS
Healing following conventional scaling and root planing
is seen clinically as a reduction in pocket depth and is
the result of a reduction in inflammation which causes
tissue shrinkage or reduced inflammatory swelling and
also an improved tissue tone. This improved tissue form
is more resistant to pocket probing forces and is detect-
ed clinically as an increase in clinical attachment. The
tissue shrinkage may result in recession which, together
with the increased attachment, produces reduced pro-
bing depths. It has been hypothesized that, in smokers,
much of the inflammatory tissue swelling before treat-
Cit ev'Ora 36
Crit Rev Oral Biol Med 361

Figure. A diagram summarizing the interactions between smoking and other factors effective in terms of probing depth reduc-
which could u[timately lead to periodontal destruction.
ment may be absent, and thus this part of the post-ther-
apy tissue change may not contribute as much to the
post-treatment pocket depth reduction in smokers com-
pared with non-smokers (Kinane and Radvar, 1997). All
things being equal, smokers could therefore have deeper
pockets after therapy than non-smokers, and these pock-
ets will continue to harbor quantitatively and qualita-
tively more pathogenic bacteria than shallower pockets.
Coupled with this are the reduced fibroblast, PMN, and
epithelial cell function, reduced host defense response,
and reduced vascularity of the site. These tissue differ-
ences in smokers following the initial short-term healing
after therapy (up to six weeks) may partly explain the dif-
ferences in treatment response.
Differences in healing in the medium to longer term
(three months to one year) may be related to the cellular
and tissue differences in smokers and may account for
the refractory nature of the disease in many smokers and
the poorer longer-term healing response reported.
Fibroblasts are an important cell in the periodontal heal-
ing response, and Raulin et al. (1988) has reported an
impaired function of fibroblasts in smokers. Fibroblasts
have been shown to bind and internalize nicotine (Hanes
et al., 1991), which may be detrimental to their function.
Poorly functioning fibroblasts may not produce collagen
362
Downloaded from cro.sagepub.com at VICTORIA UNIV LIB on June 5, 2015 For personal use only. No other uses without permission.
fibers as efficiently, and thus gingival tis-
sue support and adaptation will be
impaired or at least slowed, and poor tis-
sue form will often result in greater micro-
bial plaque retention around teeth.
Another crucial cell of the dento-gin-
gival barrier is the keratinocyte. Johnson et
al. (1996) have shown that human gingival
keratinocytes are induced to produce sig-
nificantly increased amounts of IL-1 and
prostaglandin E-2 (PGE2) by tobacco
extracts. Furthermore, a constant feature of
the junctional epithelium is the presence
of PMN migrating through the epithelial
layers and into the gingival crevice. The
PMN is considered an important cell in the
local host defense at this site. MacFarlane
et al. (1992) reported that phagocytosis of
polymorphonuclear leukocytes in refracto-
ry periodontitis patients was impaired.
They found that 90% of these patients were
smokers compared with 210% of the con-
trols. No direct assessment of smoking or
tobacco products on PMN function was
assessed, however.
Summary
In the treatment of smokers, the use of
non-surgical therapy will generally be
tion and gingivitis, albeit to a lesser
extent than with non-smokers. Similar
benefits ma' y also pertain for surgical intervention strate-
gies, but catution should be exercised in more advanced
types of surf gery, e.g., regenerative surgery. Smoking influ-
ences healirng, and therefore the capacity for regenera-
tion, particuilarly bone regeneration, may be impeded.
The effects of smoking on the outcome of periodontal
therapy
mae y be summarized as the following trends:
therm
short-term eeffects in terms of less gingivitis resolution,
less probing depth reduction, and less attachment gain
in smokers. The longer-term effects are evidenced by the
fact that 80--90% of treatment failures occur in smokers
and 70-80% ' of implant failures occur in smokers. There is
now consideLrable evidence for the role of smoking in the
etiology of p)eriodontal disease and its adverse influence
on the treat]ment of periodontitis (Fig.), such that advis-
ing patientss of the consequences of tobacco use is
essential in the management of patients who smoke.
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